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Genet. Sel. Evol. 39 (2007) 405–419 Available online at: c  INRA, EDP Sciences, 2007 www.gse-journal.org DOI: 10.1051/gse:2007011 Original article Genetic and environmental effects on semen traits in Lacaune and Manech tête rousse AI rams (Open Access publication) Ingrid D   a∗ ,XavierD b , Gilles L c , Eduardo M  a , Christèle R-G ´  a ,LoysB a a Station d’amélioration génétique des animaux, INRA, UR631, BP 52627, 31320 Castanet-Tolosan Cedex, France b Physiologie de la reproduction et des comportements, INRA - CNRS UMR1291, 37380 Nouzilly, France c Institut de l’Élevage, ANIO, BP 42118, 31320 Castanet-Tolosan Cedex, France (Received 4 May 2006; accepted 22 February 2007) Abstract – Data from 51 107 and 11 839 ejaculates collected on rams of the “Lacaune”and “Manech tête rousse” breeds, respectively, were analysed to determine environmental and ge- netic factors affecting semen production traits (ejaculate volume, semen concentration, number of spermatozoa and motility) in young ( 1 year) and adult ( 2 years) rams. Fixed effects and variance components were estimated using multiple trait animal models within each breed. For all traits, the main environmental effects identified were year, season, number of ejaculations, daily variation, interval from previous to current collection and age. Heritability estimates were moderate for volume, concentration and number of spermatozoa (0.12 to 0.33) and lower for motility (0.02 to 0.14). Genetic correlations between ages differed from 1 for all traits (0.14 to 0.90), indicating that semen characteristics corresponded to different traits in young and adult rams. Genetic and phenotypic correlations among traits within age category were globally sim- ilar for the different breeds and categories of animals. ram / semen / environmental factor 1. INTRODUCTION In the ovine species, more than 800 000 artificial inseminations (AI) are performed each year in France with fresh semen. The insemination technique is used during a limited period of the year, therefore semen production units ∗ Corresponding author: Ingrid.David@toulouse.inra.fr Article published by EDP Sciences and available at http://www.gse-journal.org or http://dx.doi.org/10.1051/gse:2007011 406 I. David et al. need to produce a large amount of useful semen per day with a limited num- ber of rams. For a given preservation technique, the number of doses produced per ejaculate depends on the volume, sperm concentration and sperm motility. These traits are affected by environmental, management, physiological status and genetic effects. The principal environmental effects reported in the lit- erature are the age of the ram, season or photoperiodic treatment, nutrition, rhythm of collection, collector and daily period [2, 4, 6, 8, 12, 15, 17, 21–23]. A wide range of genetic parameter estimates of semen traits have been reported in the literature but limited data are available for sheep [7,22]. In order to improve their efficiency, French AI centres are interested in (1) the identification of the main environmental effects affecting semen pro- duction (volume, concentration, number of spermatozoa and motility); (2) estimation of the corresponding genetic parameters; and (3) prediction of adult ( 2 years) semen production based on early production in young rams ( 1 year). To cover these requirements, a study was performed on semen pro- duction traits in both adult and young rams. This paper presents the results obtained on two sets of similar data recorded at two AI centres with different breeds: Lacaune and Manech tête rousse. 2. MATERIALS AND METHODS 2.1. Data Routine recorded semen production data were provided by two AI cen- tre members of the ANIO (association nationale des centres d’insémination ovine). Data were collected from “Lacaune” (LAC) rams during the years 1996–2004 and “Manech tête rousse” (MTR) rams during the years 2000–2004. Each breed was housed in a separate AI centre located in the southwest of France: Aveyron (LAC) and Pyrénées Atlantiques (MTR). Rams were involved in a dairy selection scheme and belonged to two categories: young rams under progeny testing and proven adult rams. Only records of ejaculates corresponding to the intensive period of ram collection (May to Au- gust), after photoperiodic treatment in one centre or a melatonin implant in the other, were used for the analysis. In total, 51 107 and 11 839 ejaculates of LAC and MTR rams were analysed, respectively. Data were collected over a 1 to 5 year period depending on the rams. The interval between collections within year varied from 1 to 28 days. Detailed data descriptions are presented in Table I. All ejaculates were obtained after natural ejaculation in an artificial vagina by the same team of collectors during the entire period. For a given ram the Genetic study of semen traits in AI sheep 407 Table I . Description of data recorded in AI centres. Center 1 Center 2 Adult Young Adult Young Volume* (mL) 0.96 (0.32) 0.67 (0.23) 1.05 (0.32) 0.58 (0.26) Concentration* (×10 6 spz·mL −1 ) 3.52 (0.69) 3.33 (0.74) 4.50 (0.80) 4.10 (0.90) Number of spermatozoa* 3.41 (1.29) 2.26 (0.97) 4.80 (1.70) 2.50 (1.30) Motility* 4.70 (0.10) 4.64 (0.12) 4.70 (0.20) 4.60 (0.30) Number of collections recorded 7328 4511 36 480 14 627 Number of rams 465 436 1880 974 Average number of records 18 (1–183) 10 (1–31) 36 (1–183) 8 (1–17) per animal (minimum-maximum) Number of sires 111 131 230 197 Number of animals in the final 5796 20 761 pedigree file * Average (s.e.). pool of 1 to 3 successive ejaculates, obtained over a 2–5 min period, was evaluated immediately after collection. Three traits were evaluated for each pool: volume which was read directly from a graduated collection tube (mL), semen concentration which was determined using a standard spectrophotome- ter (10 6 spermatozoa per mL) and mass motility which was assessed for undi- luted unstained semen under a microscope. Mass motility was scored subjec- tively, on the basis of wave motion, on a 0 (no motion) to 5 (numerous rapid and vigorous waves) continuous scale. 2.2. Models and methods Four dependent variables were analysed: the sperm concentration, ejacu- late volume defined as the pool volume divided by the number of ejaculates, number of spermatozoa computed as the product of the ejaculate volume and sperm concentration and motility. Records above the threshold of 3 mL for the ejaculate volume, 8 × 10 6 spz·mL −1 for concentration and 5 for motility were discarded; these represented 1 and 8% of the data in LAC and MTR rams, respectively. For motility, analysis was restricted to records above 4 because the scoring of a collection was not reliable below this threshold. Analysis was performed separately for each breed. Six multiple trait animal models were considered for the estimation of the genetic parameters for semen production traits within breed. The first two mod- els were multiple trait animal models (SAC model: single animal category) for semen traits in adult and young rams, respectively. The four other models (SSM model: single semen measurement) were multiple trait animal models 408 I. David et al. for each semen trait of young and adult rams. Simple repeatability models were used for all traits in all multiple trait models. The random effects ac- counted for were the additive genetic effect, permanent environmental effect and residual. The fixed effects tested, using likelihood ratio tests, were season (week or midmonth), daily variation (AM/PM), age at collection in years (for adult rams only, age = 2−7, (7)  7 years), interval from previous collection in days (interval = 1−8; (8)  8 days), number of collections sustained the previous year (for adult rams only), rank of collection within season, breeding value for milk production in quartiles and all two-way interactions with bio- logical meaning. For each model, variance and covariance components were estimated using a Restricted Maximum Likelihood method implemented in ASREML software [11] applied to multiple trait animal models. The heritabil- ity for each trait was estimated by ˆσ 2 a / ˆσ 2 T with ˆσ 2 T = ˆσ 2 a + ˆσ 2 p + ˆσ 2 e and where ˆσ 2 a , ˆσ 2 p and ˆσ 2 e are the variance estimates for additive genetic, random per- manent environmental and random residual effects respectively for each trait. Repeatability was estimated by  ˆσ 2 a + ˆσ 2 p  / ˆσ 2 T . 3. RESULTS 3.1. Analysis of fixed effects For the traits considered, the effects of the breeding value for milk produc- tion, the rank of collection within season, the number of collections sustained the previous year and all two-way interactions except season-year interaction were removed because they were not significant (P > 5%) in both breeds. The maximal variations due to the main fixed effects (in standard error unit) reach- ing significance for at least one trait are presented in Tables II and III for MTR and LAC rams, respectively. The effects of year, season and the year-season interaction were significant for all traits in both breeds. The year of collection was one of the two principal causes of variation in both breeds and for all traits. A decrease of concentra- tion with years was observed in both age categories and breeds, while for the other semen characteristics, there was no clear trend associated with year. The season effect was the principal cause of variation in nearly all cases. Volume, concentration and number of spermatozoa first increased and then decreased with season while no clear trend could be observed for motility. In adult rams, the age effect was significant for concentration and number of spermatozoa in both breeds and for volume and motility in LAC rams only. All semen production traits tended to decrease for rams older than 3 years (Fig. 1). Genetic study of semen traits in AI sheep 409 Table II. Maximum range between fixed effect estimates, in standard error unit, for each trait in Manech tête rousse rams. Volume Concentration No. of Motility spermatozoa Young Adult Young Adult Young Adult Young Adult Year 0.9 1.1 0.9 1.9 1.2 1.0 1.0 1.3 Season 1.0 1.9 1.2 1.4 1.1 1.3 0.7 0.5 Interval with previous 0.5 0.3 # 0.1 0.5 0.3 0.1 0.3 collection Number of ejaculates 0.6 0.2 0.1 0.1 0.2 0.2 # 0.1 Daily variation 0.1#####0.20.1 Age - # - 2.9 - 1.0 - # #: Not significant effect; -: not tested. Table III. Maximum range between fixed effect estimates, in standard error unit, for each trait in Lacaune rams. Volume Concentration No. of Motility spermatozoa Young Adult Young Adult Young Adult Young Adult Year 0.5 2.2 1.4 1.9 0.5 0.8 0.5 0.9 Season 1.0 0.8 1.1 1.2 0.6 0.4 0.4 0.6 Interval with previous 0.2 0.4 0.2 0.3 0.3 0.6 0.2 0.2 collection Number of ejaculates Daily variation 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 Age - 1.6 - 0.1 - 0.9 - 0.2 -: Not tested. The decrease in the number of spermatozoa with increasing age was very sim- ilar in both breeds. This was mainly due to a decrease of volume in LAC rams and a decrease of concentration in MTR rams. Except for the concentration in young MTR rams, all traits were signifi- cantly affected by the interval with previous collection in both breeds. The same trend was observed for volume, number of spermatozoa and concentra- tion (Fig. 2). They increased significantly from 0 (interval = 1) to 2 (inter- val = 3) days of abstinence, and remained stable (not significant differences) for the interval with previous collection higher than 3 days. Except for adult LAC rams, motility tended to decrease when the interval between collections increased from 1 to 4 days. The daily variation significantly affected motility traits in both breeds (Tabs. II and III). Semen production traits were only significantly affected in 410 I. David et al. * LAC=Lacaune MTR=Manech tête rousse -0.1 0 0.1 8 7654 321 adult LAC adult MTR concentration −1.60 −1.10 −0.60 −0.10 234567 motility −0.06 −0.04 −0.02 0.00 0.02 234567 volume −0.15 −0.10 −0.05 0.00 0.05 0.10 234567 number of spermatozoa −1.25 −0.75 −0.25 0.25 234567 a g e ( in y ears ) * estimate * Figure 1. Effect of age on semen production. *LAC=Lacaune MTR=Manech tête rousse concentration −0.30 −0.20 −0.10 0.00 0.10 0.20 12345678 motility −0.02 0.00 0.02 0.04 0.06 12345678 number of spermatozoa −0.80 −0.30 0.20 0.70 12345678 volume −0.12 −0.07 −0.02 0.03 0.08 12345678 -0. 1 0 0.1 8 76 54 3 21 adult LAC young LAC adult MTR young MTR interval with p revious collection ( in da y s ) estimate * * * * Figure 2. Effect of interval with previous collection on semen production. Genetic study of semen traits in AI sheep 411 Table IV. Repeatability and standard error estimates obtained with the SAC a model of semen characteristics in young and adult AI rams b . Traits Young rams Adult rams Volume 0.35 (0.01) 0.46 (0.01) LAC Concentration 0.51 (0.01) 0.52 (0.01) rams* Number of spermatozoa 0.34 (0.01) 0.42 (0.01) Motility 0.30 (0.01) 0.38 (0.01) Volume 0.39 (0.02) 0.47 (0.02) MTR Concentration 0.36 (0.02) 0.40 (0.02) rams* Number of spermatozoa 0.30 (0.02) 0.40 (0.02) Motility 0.32 (0.02) 0.45 (0.02) a Model SAC = multiple trait model within single animal category. b Standard error in brackets. *LAC= Lacaune; MTR = Manech tête rousse. LAC rams, except volume in young MTR rams. The same trend was observed for all traits: collections taken in the afternoon had better quality than those taken in the morning. The effect of the number of ejaculations for a collection was studied only in MTR rams because this number was fixed to 2 in LAC rams. This effect sig- nificantly affected volume, concentration, and motility in both young and adult rams and the number of spermatozoa in adult rams only. Volume, concentration and number of spermatozoa decreased from 1 to 2 ejaculations while motility increased. There were no significant differences between 3 and 2 ejaculations for all traits. 3.2. Repeatability and genetic parameters Repeatability estimates for each trait with the SAC model are presented in Table IV. The largest difference in repeatability estimates obtained with the SSM models never exceeded 0.01. Repeatabilities were moderate for most of the traits varying from 0.30 to 0.52 and were quite similar between breeds except for concentration. The estimates for adult rams tended to be higher than for young rams. The estimates for heritability and correlations among traits are presented in Tables V and VI for young and adult rams, respectively. As for the repeatabil- ity, the differences in heritability estimates between the SAC and SSM mod- els were small. The estimates were moderate for all traits, ranging from 0.12 to 0.33, except for motility ranging from 0.02 to 0.14. However, heritability 412 I. David et al. Table V. Estimates of genetic parameters of semen characteristics in young AI rams a . Traits Model b Volume Concentration Number of spermatozoa Motility LAC rams* Vo l u m e SAC 0.18 (0.03) 0.13 0.89 −0.03 SSM 0.19 (0.03) Concentration SAC −0.24 0.27 (0.04) 0.52 0.20 SSM 0.27 (0.04) Number of SAC 0.84 0.30 0.17 (0.03) 0.05 spermatozoa SSM 0.17 (0.03) Motility SAC −0.04 0.04 −0.01 0.07 (0.02) SSM 0.07 (0.02) MTR rams* Vo l u m e SAC 0.33 (0.07) 0.07 0.85 −0.05 SSM Concentration SAC −0.41 0.18 (0.06) 0.53 0.23 SSM 0.20 (0.05) Number of SAC 0.89 −0.27 0.19 (0.06) 0.07 spermatozoa SSM 0.18 (0.05) Motility SAC −0.03 0.44 −0.12 0.14 (0.06) SSM 0.11 (0.05) a Heritabilities (s.e.) on the diagonal, genetic and phenotypic correlations below and above the diagonal, respectively. b Model SAC = multiple trait model within single animal category. Model SSM = multiple trait model within semen measurement. *LAC = Lacaune; MTR = Manech tête rousse. estimates differed between breeds. Heritabilities tended to be smaller in young LAC rams but higher in young MTR rams. Phenotypic correlations among traits were similar in all groups (LAC, MTR, adult and young rams). The number of spermatozoa (product of volume and concentration) showed, as expected, a positive phenotypic correlation with vol- ume and concentration, but the correlation was higher with volume. Small but positive (varying from 0.01 to 0.13) phenotypic correlations were observed between volume and concentration. Motility was slightly positively correlated with concentration (0.18 to 0.23). Genetic correlations among volume and other traits were similar in all groups. Volume was strongly positively correlated with number of spermato- zoa (> 0.84), moderately and negatively correlated with concentration (−0.24 to −0.53) and only slightly negatively correlated with motility (−0.03 to −0.09). For other correlations, some differences between breeds were ob- served: concentration and number of spermatozoa were positively correlated in LAC rams (0.30: young, 0.20: adult) and negatively correlated in MTR rams (−0.27: young, −0.31: adult). Genetic study of semen traits in AI sheep 413 Table V I. Estimates of genetic parameters of semen characteristics in adult AI rams a . Traits Model b Volume Concentration Number of spermatozoa Motility LAC rams* Vo l u m e SAC 0.26 (0.04) 0.04 0.86 −0.02 SSM 0.27 (0.04) Concentration SAC −0.33 0.25 (0.05) 0.51 0.18 SSM 0.27 (0.05) Number of SAC 0.85 0.20 0.19 (0.04) 0.06 spermatozoa SSM 0.20 (0.04) Motility SAC −0.08 0.07 −0.04 0.13 (0.03) SSM 0.13 (0.03) MTR rams* Vo l u m e SAC 0.25 (0.06) 0.01 0.86 −0.08 SSM 0.30 (0.05) Concentration SAC −0.53 0.12 (0.05) 0.46 0.19 SSM 0.14 (0.05) Number of SAC 0.89 −0.31 0.14 (0.06) 0.03 spermatozoa SSM 0.18 (0.05) Motility SAC −0.09 −0.70 −0.74 0.04 (0.04) SSM 0.02 (0.04) a Heritabilities (s.e.) on the diagonal, genetic and phenotypic correlations below and above the diagonal, respectively. b Model SAC = multiple trait model within single animal category. Model SSM = multiple trait model within semen measurement. *LAC = Lacaune; MTR = Manech tête rousse. The four different correlations calculated between traits recorded for young and adult rams are presented in Table VII. Genetic correlations between age categories for each trait differed from 1. Except for motility, correlations were higher in MTR than in LAC rams. Correlations between permanent environ- mental effects of young and adult rams were low in both breeds (< 0.5). Con- sequently, the correlations of ability to produce semen (genetic additive value + permanent environmental effect) between young and adult rams were mod- erate and ranged from 0.42 to 0.81. In general, the correlations between adult ability and young genetic additive value were higher. 4. DISCUSSION The present study has the advantage of analysing several years of semen production of rams with different ages, breeds, and locations. This gives the opportunity to identify similarities and differences in semen production among time, breeds or age. 414 I. David et al. Table VII. Estimates of correlations of semen characteristics between young and adult AI rams with the SSM a model. Traits Corr 1 b Corr 2 b Corr 3 b Corr 4 b Volume 0.76 0.24 0.60 0.79 LAC Concentration 0.51 0.38 0.50 0.54 rams* Number of spermatozoa 0.52 0.33 0.50 0.56 Motility 0.81 0.41 0.62 0.76 Volume 0.90 0.37 0.81 0.78 MTR Concentration 0.89 0.27 0.53 0.60 rams* Number of spermatozoa 0.81 0.16 0.42 0.59 Motility 0.14 0.48 0.58 0.00 a Model SSM = multiple trait model within semen measurement. b Corr 1 = corr(va young, va adult); Corr 2 = corr(ep young, ep adult); Corr 3 = corr(ep + va young, ep + va adult); Corr 4 = corr(va young, ep + va adult); where va = additive genetic value, ep = permanent environmental effect. *LAC = Lacaune; MTR = Manech tête rousse. The year effect which was encountered reflected a combination of an impor- tant list of factors which may affect semen production [10, 18], some are not fully controllable by the AI centre (e.g. dryness, temperature, herd disease ) while others can be modified (e.g. nutrition, management, selection ).These factors were or could not be recorded and therefore have not been tested in the model. Explaining chaotic changes in volume and motility over the years is difficult. The decrease of the concentration may suggest a regular change of an environmental factor or an indirect response to selection on other traits. However, the same trends have been reported in humans even though they are partly controversial [16, 26]. The seasonal effect accounted for variations due to photoperiodic or mela- tonin treatments as described by Chemineau et al. [5] and Colas et al. [6] in adult rams. Sheep are short day breeders and these treatments are a substitute for decreasing day length allowing the obtention of, during the AI period, the same quantity and quality of semen as during the normal breeding season. Al- though breed, centre and seasonality treatment were confounded, melatonin implant tended to produce a shorter effect than photoperiodic treatment and was less repeatable in this study. More precisely, the season-year interaction corresponded mainly to quantitative interaction for photoperiodic treatment and qualitative interaction for melatonin implant. The seasonal variations of production traits tended to be less consistent for young than for adult rams. [...].. .Genetic study of semen traits in AI sheep 415 Indeed, for young rams the seasonal effect included daily gain which is known to affect semen traits [19, 20, 23] The age of rams affected the number of spermatozoa mainly due to effects on volume in LAC and concentration in MTR This may be explained by a difference between AI centre management or between breed in the senescence of rams The age effect on semen. .. [13, 19, 20, 23] The lack of information on daily gain in our data led us to consider that genes affecting growth may also be affecting semen production This might also explain the differences in heritability estimates between young and adult rams If available, individual body Genetic study of semen traits in AI sheep 417 growth could be taken into account as a covariate trait in a structural model which... of genetic parameters of semen production traits 5 CONCLUSION In the present study, environmental factors identified as affecting semen production showed, in general, the same trend for all categories of animals and breeds The analysis of these environmental factors may help AI centres to improve semen production even if the effect of year needs more investigation Heritabilities of semen production traits. .. were in accordance with those found in the literature [1, 22, 24] Genetic correlations between number of spermatozoa and concentration were opposed in LAC and in MTR This result is not independent of the relationship between volume and these two traits: number of spermatozoa = volume × concentration In fact, volume and number of spermatozoa were highly positively correlated and volume and concentration... correlated in both breeds but much more negative in MTR than in LAC The variability in genetic correlation estimates between motility and other traits may be explained by the subjectivity and lack of reliability of this trait We found that semen traits were genetically different between young and adult rams In our analysis, young rams were still growing which is known to have an effect on semen characteristics... impact of semen trait selection on other traits (e.g fertility, prolificacy, dairy traits, adult body size) must be evaluated beforehand ACKNOWLEDGEMENTS The authors thank the ministère de l’Agriculture for supporting this study in the frame of a “BELIA action”, directed by the ANIO and the INRA, and the AI centres who provided the data: BMC, CCDEO, Confédération générale de Roquefort, Insem-Ovin, OVI-TEST,... 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Available online at: c  INRA, EDP Sciences, 2007 www.gse-journal.org DOI: 10.1051/gse:2007011 Original article Genetic and environmental effects on semen traits in Lacaune and Manech tête rousse AI. 1 for all traits (0.14 to 0.90), indicating that semen characteristics corresponded to different traits in young and adult rams. Genetic and phenotypic correlations among traits within age category. [7,22]. In order to improve their efficiency, French AI centres are interested in (1) the identification of the main environmental effects affecting semen pro- duction (volume, concentration, number